PLD3 affects axonal spheroids and network defects in Alzheimer’s disease

The precise mechanisms that lead to cognitive decline in Alzheimer’s disease are unknown. Here we identify amyloid-plaque-associated axonal spheroids as prominent contributors to neural network dysfunction. Using intravital calcium and voltage imaging, we show that a mouse model of Alzheimer’s disea...

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Published inNature (London) Vol. 612; no. 7939; pp. 328 - 337
Main Authors Yuan, Peng, Zhang, Mengyang, Tong, Lei, Morse, Thomas M., McDougal, Robert A., Ding, Hui, Chan, Diane, Cai, Yifei, Grutzendler, Jaime
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 08.12.2022
Nature Publishing Group
Subjects
13/1
13/44
13/51
14/19
14/28
14/34
14/35
14/63
14/69
42/41
631/378/1689/1283
631/378/3920
631/378/87
64/60
Abnormalities
Accumulation
Alzheimer Disease - metabolism
Alzheimer Disease - pathology
Alzheimer's disease
Amyloid
Animals
Axon guidance
Axons - metabolism
Axons - pathology
Biosynthesis
Calcium channels (voltage-gated)
Calcium imaging
Circuits
Cognitive ability
Disease Models, Animal
Disruption
Electric currents
Electrical conduction
Humanities and Social Sciences
Mice
multidisciplinary
Neural networks
Neurodegenerative diseases
Phospholipase D - metabolism
Propagation
Science
Science (multidisciplinary)
Signal to noise ratio
Spheroids
Spheroids, Cellular - metabolism
Online AccessGet full text

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Abstract The precise mechanisms that lead to cognitive decline in Alzheimer’s disease are unknown. Here we identify amyloid-plaque-associated axonal spheroids as prominent contributors to neural network dysfunction. Using intravital calcium and voltage imaging, we show that a mouse model of Alzheimer’s disease demonstrates severe disruption in long-range axonal connectivity. This disruption is caused by action-potential conduction blockades due to enlarging spheroids acting as electric current sinks in a size-dependent manner. Spheroid growth was associated with an age-dependent accumulation of large endolysosomal vesicles and was mechanistically linked with Pld3 —a potential Alzheimer’s-disease-associated risk gene 1 that encodes a lysosomal protein 2 , 3 that is highly enriched in axonal spheroids. Neuronal overexpression of Pld3 led to endolysosomal vesicle accumulation and spheroid enlargement, which worsened axonal conduction blockades. By contrast, Pld3 deletion reduced endolysosomal vesicle and spheroid size, leading to improved electrical conduction and neural network function. Thus, targeted modulation of endolysosomal biogenesis in neurons could potentially reverse axonal spheroid-induced neural circuit abnormalities in Alzheimer’s disease, independent of amyloid removal. Amyloid-plaque-associated axonal spheroids are prominent contributors to neural network dysfunction in an Alzheimer’s model and can be reversed by endolysosomal modulation.
AbstractList The precise mechanisms that lead to cognitive decline in Alzheimer's disease are unknown. Here we identify amyloid-plaque-associated axonal spheroids as prominent contributors to neural network dysfunction. Using intravital calcium and voltage imaging, we show that a mouse model of Alzheimer's disease demonstrates severe disruption in long-range axonal connectivity. This disruption is caused by action-potential conduction blockades due to enlarging spheroids acting as electric current sinks in a size-dependent manner. Spheroid growth was associated with an age-dependent accumulation of large endolysosomal vesicles and was mechanistically linked with Pld3-a potential Alzheimer's-disease-associated risk gene1 that encodes a lysosomal protein2,3 that is highly enriched in axonal spheroids. Neuronal overexpression of Pld3 led to endolysosomal vesicle accumulation and spheroid enlargement, which worsened axonal conduction blockades. By contrast, Pld3 deletion reduced endolysosomal vesicle and spheroid size, leading to improved electrical conduction and neural network function. Thus, targeted modulation of endolysosomal biogenesis in neurons could potentially reverse axonal spheroid-induced neural circuit abnormalities in Alzheimer's disease, independent of amyloid removal.The precise mechanisms that lead to cognitive decline in Alzheimer's disease are unknown. Here we identify amyloid-plaque-associated axonal spheroids as prominent contributors to neural network dysfunction. Using intravital calcium and voltage imaging, we show that a mouse model of Alzheimer's disease demonstrates severe disruption in long-range axonal connectivity. This disruption is caused by action-potential conduction blockades due to enlarging spheroids acting as electric current sinks in a size-dependent manner. Spheroid growth was associated with an age-dependent accumulation of large endolysosomal vesicles and was mechanistically linked with Pld3-a potential Alzheimer's-disease-associated risk gene1 that encodes a lysosomal protein2,3 that is highly enriched in axonal spheroids. Neuronal overexpression of Pld3 led to endolysosomal vesicle accumulation and spheroid enlargement, which worsened axonal conduction blockades. By contrast, Pld3 deletion reduced endolysosomal vesicle and spheroid size, leading to improved electrical conduction and neural network function. Thus, targeted modulation of endolysosomal biogenesis in neurons could potentially reverse axonal spheroid-induced neural circuit abnormalities in Alzheimer's disease, independent of amyloid removal.
The precise mechanisms that lead to cognitive decline in Alzheimer's disease are unknown. Here we identify amyloid-plaque-associated axonal spheroids as prominent contributors to neural network dysfunction. Using intravital calcium and voltage imaging, we show that a mouse model of Alzheimer's disease demonstrates severe disruption in long-range axonal connectivity. This disruption is caused by action-potential conduction blockades due to enlarging spheroids acting as electric current sinks in a size-dependent manner. Spheroid growth was associated with an age-dependent accumulation of large endolysosomal vesicles and was mechanistically linked with Pld3-a potential Alzheimer's-disease-associated risk gene that encodes a lysosomal protein that is highly enriched in axonal spheroids. Neuronal overexpression of Pld3 led to endolysosomal vesicle accumulation and spheroid enlargement, which worsened axonal conduction blockades. By contrast, Pld3 deletion reduced endolysosomal vesicle and spheroid size, leading to improved electrical conduction and neural network function. Thus, targeted modulation of endolysosomal biogenesis in neurons could potentially reverse axonal spheroid-induced neural circuit abnormalities in Alzheimer's disease, independent of amyloid removal.
The precise mechanisms that lead to cognitive decline in Alzheimer’s disease are unknown. Here we identify amyloid-plaque-associated axonal spheroids as prominent contributors to neural network dysfunction. Using intravital calcium and voltage imaging, we show that a mouse model of Alzheimer’s disease demonstrates severe disruption in long-range axonal connectivity. This disruption is caused by action-potential conduction blockades due to enlarging spheroids acting as electric current sinks in a size-dependent manner. Spheroid growth was associated with an age-dependent accumulation of large endolysosomal vesicles and was mechanistically linked with Pld3 —a potential Alzheimer’s-disease-associated risk gene 1 that encodes a lysosomal protein 2,3 that is highly enriched in axonal spheroids. Neuronal overexpression of Pld3 led to endolysosomal vesicle accumulation and spheroid enlargement, which worsened axonal conduction blockades. By contrast, Pld3 deletion reduced endolysosomal vesicle and spheroid size, leading to improved electrical conduction and neural network function. Thus, targeted modulation of endolysosomal biogenesis in neurons could potentially reverse axonal spheroid-induced neural circuit abnormalities in Alzheimer’s disease, independent of amyloid removal.
The precise mechanisms that lead to cognitive decline in Alzheimer's disease are unknown. Here we identify amyloid-plaque-associated axonal spheroids as prominent contributors to neural network dysfunction. Using intravital calcium and voltage imaging, we show that a mouse model ofAlzheimer's disease demonstrates severe disruption in long-range axonal connectivity. This disruption is caused by action-potential conduction blockades due to enlarging spheroids acting as electric current sinks in a size-dependent manner. Spheroid growth was associated with an age-dependent accumulation of large endolysosomal vesicles and was mechanistically linked with Pld3-a potential Alzheimer's-disease-associated risk gene1 that encodes a lysosomal protein2,3 that is highly enriched in axonal spheroids. Neuronal overexpression of Pld3 led to endolysosomal vesicle accumulation and spheroid enlargement, which worsened axonal conduction blockades. By contrast, Pld3 deletion reduced endolysosomal vesicle and spheroid size, leading to improved electrical conduction and neural network function. Thus, targeted modulation of endolysosomal biogenesis in neurons could potentially reverse axonal spheroidinduced neural circuit abnormalities in Alzheimer's disease, independent of amyloid removal.
The precise mechanisms that lead to cognitive decline in Alzheimer’s disease are unknown. Here we identify amyloid-plaque-associated axonal spheroids as prominent contributors to neural network dysfunction. Using intravital calcium and voltage imaging, we show that a mouse model of Alzheimer’s disease demonstrates severe disruption in long-range axonal connectivity. This disruption is caused by action-potential conduction blockades due to enlarging spheroids acting as electric current sinks in a size-dependent manner. Spheroid growth was associated with an age-dependent accumulation of large endolysosomal vesicles and was mechanistically linked with Pld3 —a potential Alzheimer’s-disease-associated risk gene 1 that encodes a lysosomal protein 2 , 3 that is highly enriched in axonal spheroids. Neuronal overexpression of Pld3 led to endolysosomal vesicle accumulation and spheroid enlargement, which worsened axonal conduction blockades. By contrast, Pld3 deletion reduced endolysosomal vesicle and spheroid size, leading to improved electrical conduction and neural network function. Thus, targeted modulation of endolysosomal biogenesis in neurons could potentially reverse axonal spheroid-induced neural circuit abnormalities in Alzheimer’s disease, independent of amyloid removal. Amyloid-plaque-associated axonal spheroids are prominent contributors to neural network dysfunction in an Alzheimer’s model and can be reversed by endolysosomal modulation.
Author Chan, Diane
Zhang, Mengyang
Morse, Thomas M.
Grutzendler, Jaime
Yuan, Peng
Tong, Lei
McDougal, Robert A.
Cai, Yifei
Ding, Hui
Author_xml – sequence: 1
  givenname: Peng
  orcidid: 0000-0003-4051-4447
  surname: Yuan
  fullname: Yuan, Peng
  organization: Department of Neurology, Yale University, Department of Rehabilitation Medicine, Huashan Hospital, State Key Laboratory of Medical Neurobiology, Institute for Translational Brain Research, MOE Frontiers Center for Brain Science, Fudan University
– sequence: 2
  givenname: Mengyang
  orcidid: 0000-0002-9544-8099
  surname: Zhang
  fullname: Zhang, Mengyang
  organization: Department of Neurology, Yale University, Department of Neuroscience, Yale University, Interdepartmental Neuroscience Program, Yale University, Department of Molecular and Cellular Physiology, Stanford University
– sequence: 3
  givenname: Lei
  surname: Tong
  fullname: Tong, Lei
  organization: Department of Neurology, Yale University
– sequence: 4
  givenname: Thomas M.
  orcidid: 0000-0002-2902-8272
  surname: Morse
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– sequence: 6
  givenname: Hui
  surname: Ding
  fullname: Ding, Hui
  organization: Department of Neurology, Yale University, Department of Neurology, Xiangya Hospital, Central South University
– sequence: 7
  givenname: Diane
  surname: Chan
  fullname: Chan, Diane
  organization: Department of Neurology, Massachusetts General Hospital
– sequence: 8
  givenname: Yifei
  surname: Cai
  fullname: Cai, Yifei
  organization: Department of Neurology, Yale University
– sequence: 9
  givenname: Jaime
  orcidid: 0000-0002-5000-243X
  surname: Grutzendler
  fullname: Grutzendler, Jaime
  email: jaime.grutzendler@yale.edu
  organization: Department of Neurology, Yale University, Department of Neuroscience, Yale University, Wu Tsai Institute, Yale University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/36450991$$D View this record in MEDLINE/PubMed
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SSID ssj0005174
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Snippet The precise mechanisms that lead to cognitive decline in Alzheimer’s disease are unknown. Here we identify amyloid-plaque-associated axonal spheroids as...
The precise mechanisms that lead to cognitive decline in Alzheimer's disease are unknown. Here we identify amyloid-plaque-associated axonal spheroids as...
SourceID pubmedcentral
proquest
pubmed
crossref
springer
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StartPage 328
SubjectTerms 13/1
13/44
13/51
14/19
14/28
14/34
14/35
14/63
14/69
42/41
631/378/1689/1283
631/378/3920
631/378/87
64/60
Abnormalities
Accumulation
Alzheimer Disease - metabolism
Alzheimer Disease - pathology
Alzheimer's disease
Amyloid
Animals
Axon guidance
Axons - metabolism
Axons - pathology
Biosynthesis
Calcium channels (voltage-gated)
Calcium imaging
Circuits
Cognitive ability
Disease Models, Animal
Disruption
Electric currents
Electrical conduction
Humanities and Social Sciences
Mice
multidisciplinary
Neural networks
Neurodegenerative diseases
Phospholipase D - metabolism
Propagation
Science
Science (multidisciplinary)
Signal to noise ratio
Spheroids
Spheroids, Cellular - metabolism
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Title PLD3 affects axonal spheroids and network defects in Alzheimer’s disease
URI https://link.springer.com/article/10.1038/s41586-022-05491-6
https://www.ncbi.nlm.nih.gov/pubmed/36450991
https://www.proquest.com/docview/2748887026
https://www.proquest.com/docview/2744667352
https://pubmed.ncbi.nlm.nih.gov/PMC9729106
Volume 612
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